Transient induction of the MRP/GS-X pump and γ-glutamylcysteine synthetase by 1-(4-amino-2-methyl-5-pyrimidinyl)methyl-3-(2-chloroethyl)-3- nitrosourea in human glioma cells

Cancer Research

Volumn 57, Issue 23, 1997, Pages 5292-5299

  Gomi, Akira ^a,b   Shinoda, Souji ^b   Masuzawa, Toshio ^b   Ishikawa, Toshihisa ^c   Kuo, M Tien ^a,d  

^a UNIVERSITY OF TEXAS   (United States)

^b JICHI MEDICAL UNIVERSITY   (Japan)

^c PFIZER INC   (United States)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENATE SODIUM; GAMMA GLUTAMYLCYSTEINE; NITROSOUREA DERIVATIVE;

ANTINEOPLASTIC ACTIVITY; ARTICLE; ENZYME INDUCTION; GENE EXPRESSION; GLIOMA; GLUTATHIONE METABOLISM; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MULTIDRUG RESISTANCE; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES; ANTINEOPLASTIC AGENTS; ARSENATES; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CISPLATIN; DOXORUBICIN; DRUG RESISTANCE, MULTIPLE; ENZYME INDUCTION; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOMA; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; HUMANS; LEUKOTRIENE C4; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED BALB C; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NIMUSTINE; PEPTIDE FRAGMENTS; RNA, MESSENGER; TRANSCRIPTION, GENETIC; TUMOR CELLS, CULTURED;

EID: 0030697927     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (58)

1. Takakura, K., Abe, H., Tanaka, R., Kitamura, K., Miwa, T., Takeuchi, K., Yamamoto, S., Kageyama, N., Handa, H., Mogami, H., Nishimoto, A., Uozumi, T., Matsutani, M., and Nomura, K. Effects of ACNU and radiotherapy on malignant glioma. J. Neurosurg., 64: 53-57, 1986.
2. Walker, M. D., Green, S. B., Byar, D. P., Alexander, E., Batzdorf, U., Brooks, W. H., Hunt, W., MacCarty, C. S., Mahaley, M. S., Mealey, J., Owens, G., Ransohoff, J., II, Robertson, J. T., Shapiro, W. R., Smith, K. R., Wilson, C. B., and Strike, T. A. Randomized comparison of radiotherapy and nitrosoureas for the treatment of malignant glioma after surgery. N. Engl. J. Med., 303: 1323-1329, 1980.
3. Aida, T., and Bodell, W. J. Cellular resistance to chloroethylnitrosoureas, nitrogen mustard, and cis-diamminedichloroplatinum(II) in human glial-derived cell lines. Cancer Res., 47: 1361-1366, 1987.
4. Kohn, K. W. Interstrand cross-linking of DNA by 1,3-bis(2-chloroethyl)-1-nitrosourea and other 1-(2-haloethyl)-1-nitrosourea. Cancer Res., 37: 1450-1454, 1977.
5. Erickson, L. C., Laurent, G., Sharkey, N. A., and Kohn, K. W. DNA cross-linking and monoadduct repair in nitrosourea-treated human tumour cells. Nature (Lond.), 288: 727-729, 1980.
6. 6-methylguanine-DNA methyltransferase. Nucleic Acids Res., 11: 7743-7758, 1983.
7. 6-alkylguanine-DNA alkyltransferase: regulation and importance in response to alkylating carcinogenic and therapeutic agents. Cancer Res., 50: 6119-6129, 1990.
8. Gomi, A., Shinoda, S., Sakai, R., Hirai, H., Ozawa, K., and Masuzawa, T. Elevated expression of DNA polymerase β gene in glioma cell lines with acquired resistance to 1-(4-amino-2-methyl-5-pyrimidinyl)methyl-3-(2-chloroethyl)-3-nitrosourea. Biochem. Biophys. Res. Commun., 227: 558-563, 1996.
9. Cole, S. P. C., Bhardwaj, G., Gerlach, J. H., Mackie, J. E., Grant, C. E., Almquist, K. C., Stewart, A. J., Kurz, E. U., Duncan, A. M. V., and Deeley, R. G. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science (Washington DC), 258: 1650-1654, 1992.
10. Cole, S. P. C., Sparks, K. E., Fraser, K., Loe, D. W., Grant, C. E., Wilson, G. M., and Deeley, R. G. Pharmacological characterization of multidrug resistant MRP-transfected human tumor cells. Cancer Res., 54: 5902-5910, 1994.
11. Grant, C. E., Valdimarsson, G., Hipfner, D. R., Almquist, K. C., Cole, S. P. C., and Deeley, R. G. Overexpression of multidrug resistance-associated protein (MRP) increase resistance of natural product drugs. Cancer Res., 54: 357-361, 1994.
12. Zaman, G. J. R., Flens, M. J., van Leusden, M. R., de Haas, M., Mülder, H. S., Lankelma, J., Pinedo, H. M., Scheper, R. J., Baas, F., Broxterman, H. J., and Borst, P. The human multidrug resistance-associated protein MRP is a plasma membrane drug-efflux pump. Proc. Natl. Acad. Sci. USA, 91: 8822-8826, 1994.
13. Müller, M., Meijer, C., Zaman, G. J. R., Borst, P., Scheper, R. J., Mulder, N. H., de Vries, E. G. E., and Jansen, P. L. M. Overexpression of the gene encoding the multidrug resistance-associated protein results in increased ATP-dependent glutathione S-conjugate transport. Proc. Natl. Acad. Sci. USA, 91: 13033-13037, 1994.
14. 4 and structurally related conjugates. J. Biol. Chem., 269: 27807-27810, 1994.
15. Jedlitschky, G., Leier, I., Buchholz, U., Barnouin, K., Kurz, G., and Keppler, D. Transport of glutathione, glucuronate, and sulfate conjugates by the MRP gene-encoded conjugate export pump. Cancer Res., 56: 988-994, 1996.
16. 4 and chemotherapeutic agents in membrane vesicles, demonstration of glutathione-dependent vincristine transport. J. Biol. Chem., 271: 9675-9682, 1996.
17. Loe, D. W., Almquist, K. C., Cole, S. P. C., and Deeley, R. G. ATP-dependent 17β-estradiol 17-(β-D-glucuronide) transport by multidrug resistance protein (MRP). J. Biol. Chem., 271: 9683-9689, 1996.
18. Ishikawa, T. The ATP-dependent glutathione S-conjugate export pump. Trends Biochem. Sci., 17: 463-468, 1992.
19. Ishikawa, T., Bao, J. J., Yamane, Y., Akimaru, K., Frindrich, K., Wright, C. D., and Kuo, M. T. Coordinated induction of MRP/GS-X pump and γ-glutamylcysteine synthetase by heavy metals in human leukemia cells. J. Biol. Chem., 271: 14981-14988, 1996.
20. Meister, A. Glutathione metabolism and its selective modification. J. Biol. Chem., 263: 17205-17208, 1988.
21. Zaman, G. J. R., Lankelma, J., van Telligen, O., Beijnen, J., Dekker, H., Paulusma, C., Oude Elferink, R. P. J., Baas, F., and Borst, P. Role of glutathione in the export of compounds from cells by the multidrug-resistance-associated protein. Proc. Natl. Acad. Sci. USA, 92: 7690-7694, 1995.
22. Kuo, M. T., Bao, J. J., Curley, A., Ikeguchi, M., Johnston, D. A., and Ishikawa, T. Frequent coordinated Overexpression of the MRP/GS-X pump and γ-glutamylcysteine synthetase genes in human colorectal cancers. Cancer Res., 56: 3642-3644, 1996.
23. Chomczynski, P., and Sacchi, N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem., 162: 156-159, 1987.
24. Gunning, P., Ponte, P., Okayama, H., Engel, J., Blau, H., and Kedes, L. Isolation and characterization of full-length cDNA clones for human alpha-, beta-, and gammaactin mRNAs: skeletal but not cytoplasmic actins have an ammino-terminal cysteine that is subsequently removed. Mol. Cell. Biol., 3: 787-795, 1983.
25. Ishikawa, T., Wright, C. D., and Ishizuka, H. GS-X is functionally overexpressed in cis-diamminedichloroplatinum(II)-resistant human leukemia HL-60 cells and down regulated by cell differentiation. J. Biol. Chem., 269: 29085-29093, 1994.
26. 2+-dependent cardiac transport system for glutathione S-conjugate. J. Biol. Chem., 264: 17343-17348, 1989.
27. Gripp, J. J., Chang, C., and Mulcahy, R. T. Cloning and nucleotide sequence of a full length cDNA for human liver gamma-glutamylcysteine synthetase. Biochem. Biophys. Res. Commun., 185: 29-35, 1992.
28. Tietze, F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione. Anal. Biochem., 27: 502-522, 1969.
29. Ishikawa, T., and Sies, H. Cardiac transport of glutathione disulfide and S-conjugate. J. Biol. Chem., 259: 3838-3843, 1984.
30. Kuo, M. T., Bao, J-J., Furuichi, M., Yamane, Y., Gomi, A., Savaraj, N., Masuzawa, T., and Ishikawa, T. Frequent coexpression of MRP/GS-X pump and γ-glutamylcysteine synthetase mRNA in drug-resistant cells, untreated tumor cells, and normal mouse tissue. Biochem. Pharmacol., in press, 1997.
31. Roelofsen, H., Vos, T. A., Schippers, I. J., Knipers, F., Koning, H., Moshago, H., Jansen, P. L. M., and Müller, M. Increased levels of the multidrug resistance protein in lateral membranes of proliferating hepatocyte-derived cells. Gastroenterology, 112: 511-521, 1997.
32. Huang, C-S., Chang, L-S., Anderson, M. E., and Meister, A. Catalytic and regulatory properties of the heavy subunit of rat kidney γ-glutamylcysteine synthetase. J. Biol. Chem., 268: 19675-19680, 1993.
33. Day, R. S., Miyakoshi, J., Dobler, K., Allalunis-Turner, J., McKean, J. D. S., Petruk, K., Allen, P. B. R., Aronyk, K. N., Weir, B., Buyser-Wierenga, D., Fulton, D., and Urtasun, R. C. In: M. W. Lambert and J. Laval (eds.), DNA Repair Mechanisms and Their Biologic Implications in Mammalian Cells, pp. 83-99. New York: Plenum Publishing Corp., 1989.
34. 6-benzylguanine on the sensitivity of human tumor xenografts to 1,3-bis(2-chloroethyl)-1-nitrosourea and on DNA interstrand cross-link. Cancer Res., 52: 1171-1175, 1992.
35. Sariban, E., Kohn, K. W., Zlotogorski, C., Laurent, G., D'Incalci, M., Day, R., III, Smith, B., Kornblith, P. L., and Erickson, L. C. DNA cross-linking responses of human malignant glioma cell strains to chloroethylnitrosoureas, cisplatin, and diaziquone. Cancer Res., 47: 3988-3994, 1987.
36. 6-benzylguanine combined with streptozotocin treatment enhances 1,3-bis(2-chloroethyl)-1-nitrosourea cytotoxicity. Cancer Res., 54: 4371-4375, 1994.
37. Sobol, R. W., Horton, J. K., Kühn, R., Gu, H., Singhal, R. K., Prasad, R., Rajewsky, K., and Wilson, S. H. Requirement of mammalian DNA polymerase-β in base-excision repair. Nature (Lond.), 379: 183-186, 1996.
38. Ishikawa, T., and Ali-Osman, F. Glutathione conjugation and ATP-dependent export of anticancer drugs. In: N. H. Georgopapadakou (eds.), Drug Transport in Antimicrobial and Anticancer Chemotherapy, pp. 577-612. New York: Marcel Dekker, 1995.
39. Mulcahy, R. T., Bailey, H. H., and Gipp, J. J. Transfection of complementary DNAs for the heavy and light subunits of human γ-glutamylcysteine synthetase results in an elevation of intracellular glutathione and resistance to melphalan. Cancer Res., 55: 4771-4775, 1995.
40. Kotoh, S., Naito, S., Yokomizo, A., Kohno, K., Kuwano, M., and Kumazawa, J. enhanced expression of γ-glutamylcysteine synthetase and glutathione S-transferase genes in cisplatin-resistant bladder cancer cells with multirug resistance phenotype. J. Urol., 157: 1054-1059, 1997.
41. Godwin, A. K., Meister, A., O'Dwyer, P. J., Huang, C. S., Hamilton, T. C., and Anderson, M. E. High resistance to cisplatin in human ovarian cancer cell lines is associated with marked increase of glutathione synthesis. Proc. Natl. Acad. Sci. USA, 89: 3070-3074, 1992.
42. Dusre, L., Mimnaugh, E. C., Myers, C. E., and Sinha, B. K. Potentiation of doxorubicin cytotoxicity by buthionine sulfoximine in multidrug-resistant human breast tumor cells. Cancer Res., 49: 511-515, 1989.
43. Shi, M. M., Kugelman, A., Iwamoto, T., Tian, L., and Forman, J. Quinone-induced oxidative stress elevates glutathione and induces γ-glutamylcysteine synthetase activity in rat lung epithelial L2 cells. J. Biol. Chem., 269: 26512-26517, 1994.
44. Shi, M. M., Iwamoto, T., and Forman, H. J. γ-Glutamylcysteine synthetase and GSH increase in quinone-induced oxidative stress in BPAEC. Am. J. Physiol., 267: L414-L421, 1994.
45. Favreau, L. V., and Pickett, C. B. Transcriptional regulation of the rat NAD(P)H: quinone reductase gene. J. Biol. Chem., 268: 19875-19881, 1993.
46. Prochaska, H. J., De Long, M. J., and Talalay, P. On the mechanism of induction of cancer-protective enzymes: a unifying proposal. Proc. Natl. Acad. Sci. USA, 82: 8232-8236, 1995.
47. Colinas, R. J., Hunt, D. H., Walsh, A. C., and Lawrence, D. A. Hydroquinone resistance in a murine myeloblastic leukemia cell line. Biochem. Pharmacol., 52: 945-956, 1996.
48. Powis, G., Briehl, M., and Oblong, J. Redox signaling and the control of cell growth and death. Pharmacol. Ther., 68: 149-173, 1995.
49. Wu, A-L., and More-Rowley, W. S. GSH1, which encodes γ-glutamylcysteine synthetase, is a target gene for the yAP-1 transcriptional regulation. Mol. Cell. Biol., 14: 5832-5839, 1994.
50. Szczypka, M. S., Wemmie, J. A., Moye-Rowley, W. S., and Thiele, D. J. A yeast metal resistance protein similar to human cystic fibrosis transmembrane conductance regulator (CFTR) and multidrug resistance-associated protein. J. Biol. Chem., 269: 22853-22857, 1994.
51. Li, Z-S., Szczypka, M., Lu, Y-P., Thiele, D. J., and Rea, P. A. The yeast cadmium factor protein (YCF1) is a vacuolar glutathione S-conjugate pump. J. Biol. Chem., 271: 6509-6517, 1996.
52. Wemmie, J. A., Wu, A-L., Harshman, K. D., Parker, C. S., and Moye-Rowley, W. S. Transcriptional activation mediated by the yeast AP-1 protein is required for normal cadmium tolerance. J. Biol. Chem., 269: 14690-14697, 1994.
53. Zhu, Q., and Center, M. S. Cloning and sequence analysis of the promoter region of the MRP gene of HL60 cells isolated for resistance to Adriamycin. Cancer Res., 54: 4488-4492, 1994.
54. Yao, K-S., Godwin, A. K., Johnson, S. W., Ozols, R. F., O'Dwyer, P. J., and Hamilton, T. C. Evidence for altered regulation of γ-glutamylcysteine synthetase gene expression among cisplatin-sensitive and cisplatin-resistant human ovarian cancer cell lines. Cancer Res., 55: 4367-4374, 1994.
55. Mulcahy, R. T., and Gipp, J. J. Identification of a putative antioxidant response element in the 5′-flanking region of the human γ-glutamylcysteine synthetase heavy subunit gene. Biochem. Biophys. Res. Commun., 209: 227-233, 1995.
56. Mulcahy, R. T., Wartman, M. R., Beiley, H. H., and Gipp, J. J. Constitutive and β-naphthoflovane induced expression of the human γ-glutamylcysteine synthetase heavy subunit gene is regulated by a distal antioxidant response element/TRE sequence. J. Biol. Chem., 272: 7445-7454, 1997.
57. Sekhar, K. R., Long, M., Long, J., Xu, Z-O, Summar, M. L., and Freeman, M. L. Alteration of transcriptional and post-transcriptional expression of gamma-glutamylcysteine synthetase by diethyl maleate. Radiat. Res., 147: 592-597, 1997.
58. Gottesman, M. M., and Pastan, I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu. Rev. Biochem., 62: 385-421, 1993.